Abstract
The evolution of the adaptive immune system has provided vertebrates with a uniquely sophisticated immune toolkit, enabling them to mount precise immune responses against a staggeringly diverse range of antigens. Like other vertebrates, teleost fishes possess a complex and functional adaptive immune system; however, our knowledge of the complex antigen-receptor genes underlying its functionality has been restricted to a small number of experimental and agricultural species, preventing systematic investigation into how these crucial gene loci evolve. Here, we analyse the genomic structure of the immunoglobulin heavy chain (IGH) gene loci in the cyprinodontiforms, a diverse and important group of teleosts present in many different habitats across the world. We reconstruct the complete IGH loci of the turquoise killifish (Nothobranchius furzeri) and the southern platyfish (Xiphophorus maculatus) and analyse their in vivo gene expression, revealing the presence of species-specific splice isoforms of transmembrane IGHM. We further characterize the IGH constant regions of 10 additional cyprinodontiform species, including guppy, Amazon molly, mummichog and mangrove killifish. Phylogenetic analysis of these constant regions suggests multiple independent rounds of duplication and deletion of the teleost-specific antibody class IGHZ in the cyprinodontiform lineage, demonstrating the extreme volatility of IGH evolution. Focusing on the cyprinodontiforms as a model taxon for comparative evolutionary immunology, this work provides novel genomic resources for studying adaptive immunity and sheds light on the evolutionary history of the adaptive immune system.
Highlights
The evolution of the adaptive immune system has provided vertebrates with a uniquely sophisticated immune toolkit, enabling them to mount precise immune responses against a staggeringly diverse range of antigens
The results revealed that the two species used different exon configurations for IGHM-TM: in X. maculatus, the standard teleost five-exon configuration was used, while N. furzeri used the unusual four-exon configuration seen in medaka, demonstrating that both configurations persist among the cyprinodontiforms
The presence of multiple IGHZ constant regions in X. maculatus strongly implied that the absence of this isotype in medaka and N. furzeri is the result of two independent deletion events
Summary
In order to assemble and characterize the IGH loci in N. furzeri and X. maculatus, published IGH gene segments from zebrafish [9], medaka [10] and stickleback [11,12] were aligned to the most recent genome assemblies of N. furzeri and X. maculatus (Material and methods). In X. maculatus, a single promising region was identified on chromosome 16, while in the N. furzeri genome a single region on chromosome 6 and a number of unaligned scaffold sequences were identified as potentially containing parts of the locus (electronic supplementary material, table S2). The resulting BAC inserts were integrated with the identified genome scaffolds (electronic supplementary material, figure S7) to produce a single, contiguous locus sequence, on which IGH gene segments were identified through more stringent alignment to sequences from reference species (electronic supplementary material, figure S7). The two loci differ markedly in organization and content: while the N. furzeri locus comprises two distinct subloci on opposite strands (IGH1 and IGH2, figure 2a and electronic supplementary material, figure S1), that of X. maculatus forms a single long configuration without any additional subloci (figure 2b).
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